Salivary testosterone among men was linked to concurrent sex partners & masturbation; among women, Sal-T was positively associated with masturbation; gay women, in addition, with partnered sex

Salivary Testosterone and Sexual Function and Behavior in Men and Women: Findings from the Third British National Survey of Sexual Attitudes and Lifestyles (Natsal-3). W. G. Macdowall et al. The Journal of Sex Research, Oct 11 2021. https://doi.org/10.1080/00224499.2021.1968327

Abstract: Using data from the third British National Survey of Sexual Attitudes and Lifestyles (Natsal-3) we examined associations between salivary testosterone (Sal-T) and sexual function and behavior. Single morning saliva samples were self-collected from a subsample of participants aged 18–74 years and analyzed using mass spectrometry. 1,599 men and 2,123 women were included in the analysis (40.6% of those invited to provide a sample). We adjusted for confounders in a stepwise manner: in model 1 we adjusted for age only; model 2 for age, season and relationship status, and model 3 we added BMI and self-reported health. In the fully adjusted models, among men, Sal-T was positively associated with both partnered sex (vaginal sex and concurrent partners) and masturbation. Among women, Sal-T was positively associated with masturbation, the only association with partnered sex was with ever experience of same-sex sex. We found no clear association between Sal-T and sexual function. Our study contributes toward addressing the sparsity of data outside the laboratory on the differences between men and women in the relationship between T and sexual function and behavior. To our knowledge, this is the first population study, among men and women, using a mass spectrometry Sal-T assay to do so.

Discussion

To our knowledge, this is the first population level study, of both men and women, using a validated salivary measure to explore the associations between Sal-T and aspects of sexual function and behavior.

We found no clear associations in our data between Sal-T and either overall sexual function (as measured by the Natsal-SF) or individual problems with sexual response in men or women. Among women, our data showed solitary sex to be more strongly associated than partnered sex with Sal-T; levels of Sal-T were higher in those who masturbated more recently and more frequently. We found no association between Sal-T and heterosexual partnered sexual activity among women, as measured by occurrence of vaginal sex in the past month, and nor did we find an association with number of partners or concurrency. The only measure of partnered sex associated with Sal-T among women was ever experience of same-sex behavior.

Among men, Sal-T was associated with masturbation but not more strongly than it was with partnered sex. Associations were seen between higher levels of Sal-T and recent occurrence of heterosexual partnered sex and with concurrency of sexual partners in the last five years, but not with number of sexual partners. The association with concurrency was reflected in men’s attitudes toward ‘casual’ sexual encounters, which were similarly linked with higher levels of Sal-T.

Contextualization and Interpretation

The absence of an association between T and overall sexual function in men in our large dataset is unsurprising given the measure of overall sexual function used in Natsal-3 which, as indicated above, took account not only of individual problems with response, but also the relational context, which is heavily influenced by psychosocial factors. The absence of any association with individual aspects of sexual function (erectile difficulties, lacking enjoyment in sex, distress about sex life, lacking interest in sex) is perhaps more surprising. The dominant narrative assumes T is the ‘biological driver’ of sexual desire in men. The fact that men have both higher levels of T and report higher levels of interest in sex than women seems to speak to this narrative (van Anders, 2012). Much of the evidence linking T with sexual desire in men has, however, come from clinical studies among those with overt T deficiency in the context of investigating the effects of TRT (Corona et al., 2017). There is little empirical evidence (van Anders, 2012), including that now provided by our study that T levels in men within the normal range are associated with sexual desire. In the European Male Aging Study (EMAS), which focused specifically on older men – though like Natsal drew on a large sample of community dwelling individuals – only weak associations were found between aspects of sexual function and T. These included ‘overall sexual function’ (O’Connor et al., 2011) and erectile dysfunction and frequency of both sexual thoughts and morning erections, though the associations with these latter three sexual symptoms were attenuated when adjustments were made for age, BMI, and co-existing health conditions (Wu et al., 2010). Further, the findings from EMAS highlight the non-linear relationship between T and aspects of sexual function and point to symptom-specific T ‘thresholds’; only under the ‘threshold’ does the probability of experiencing the sexual symptom increase (O’Connor et al., 2011; Wu et al., 2010). Hence, among older men, androgen deficiency is only likely to be a key pathogenic component in problems of sexual function when T levels are overtly subnormal (Wu et al., 2010). In older men with unequivocal age-related hypogonadism, TRT has been associated with modest improvements in sexual function (Matsumoto, 2019; Snyder et al., 2016). Evidence of the value of T supplementation for ‘low T’ within the normal range as a therapeutic solution to problems, such as erectile dysfunction and low libido, however, is lacking (Huo et al., 2016).

The few large community studies that have been conducted in women have identified associations between androgens and sexual function though in unadjusted analyses (Davis et al., 2005), or among women in menopausal transition (Randolph et al., 2015). In our unadjusted model, we did find an association between Sal-T and sexual desire in women, which remained significant after adjustment for age (with women lacking interest in sex having lower Sal-T than those who did not) but was attenuated after further adjustments for relationship status, season, BMI, and general health status, highlighting the importance of contextual factors. The current global consensus is that there is insufficient evidence regarding the use of T for the treatment of sexual function in premenopausal women, but among postmenopausal women T may yield benefits in terms of increasing sexual desire (as well as other components of sexual function including arousal and orgasmic function) (Davis et al., 2019). Evidence from controlled trials among postmenopausal women indicates that estrogen-only therapies are also associated with increases in sexual desire and that these effects can be enhanced when estrogen is coupled with T (Cappelletti & Wallen, 2016).

Our data support our prior assumption that the relative influence of hormonal status and social context, and hence the strength of associations between Sal-T and sexual behavior, would vary between men and women. Attempts to understand why dyadic sex, especially partner concurrency, is more strongly associated with T among men than women have drawn on evolutionary theories asserting that it may have greater reproductive advantage for men (Puts et al., 2015; van Anders et al., 2015). Yet associations between T and dyadic and solo sex may also be differentially moderated in men and women by gendered social norms regulating sexual behavior (van Anders et al., 2015). Variation in the extent to which men and women may be differentially socialized to non-exclusivity features regularly in explanations as to why men report larger numbers of sexual partners than women in research (Jonason & Fisher, 2009; Mitchell et al., 2019).

Sal-T’s marked link with masturbation among women, in the absence of an observed link with aspects of partnered behavior, may be seen as consistent with the notion of a stronger moderating effect of social factors on hormonal influences on women’s behavior. It has been proposed that masturbation may be a ‘truer’ measure of sexual desire, as although socially censured, it is neither constrained by social surveillance nor dependent on social relations. The suggestion in our data of a stronger link with solitary than partnered sexual activity among women accords with evidence reported elsewhere; albeit from either laboratory studies and/or those utilizing smaller convenience samples (Randolph et al., 2015; van Anders, 2012). Interpretation of these findings has drawn on the bi-directionality of the association between T and sexuality (Goldey & van Anders, 2011) and on the different meanings and motivations attached to solitary and partnered sex. For example, qualitative research among women points to solitary sexuality as primarily erotic and partnered sexuality as nurturant (Goldey et al., 2016). Women self-identifying as heterosexual have been shown to be more likely to reach orgasm in solitary compared with partnered sex (Carvalheira & Leal, 2013) and the experience of orgasm has been found to increase levels of T (van Anders et al., 2007).

Our finding of higher mean Sal-T in women with ever experience of same sex sex is illuminated by a recent systematic review, investigating whether lesbian and bisexual women may have different levels of sex hormones compared to heterosexual women. The review found tentative evidence of higher T among sexual minority women, though the heterogeneity of studies and problems with confounding made it hard to draw definitive conclusions (Harris et al., 2020).

Strengths and Weaknesses

This study had a number of strengths. Firstly, Natsal-3 is a large population-based study of men and women, covering a wide age range and capturing multiple aspects of sexual function, behavior, and attitudes. Secondly, Sal-T was measured by the ‘gold standard’ method of mass spectrometry using samples collected at the same time of day in order to account for the diurnal variation in testosterone. Thirdly, we were able to adjust for known confounders identified in our earlier analysis (Clifton et al., 2016; Keevil et al., 2017), so that independent associations between Sal-T and sexual function and behavior could be established. A number of limitations need also to be considered. Firstly, nonparticipation bias is likely to have occurred both in relation to recruitment to the main survey and providing a saliva sample. There were known differences between those who did and did not return a saliva sample, though statistical weighting was used to minimize these biases. The second limitation is that, with the exception of items relating to appraisal of sex life, the Natsal-SF (which included the questions about the individual problems with sexual response) was only asked of people who were sexually active in the past year and so excluded those who may not have had sex in over a year because of sexual difficulties. The third limitation relates to the adjustments made. While we did adjust for variables identified from our previous analyses as linked with both Sal-T and sexual function and behavior (Clifton et al., 2016; Keevil et al., 2017) there are, however, likely to be other confounders that we have not adjusted for. A further limitation relates to the complexity of the phenomena under investigation and the challenge in establishing causal direction when using cross-sectional data and single saliva samples given evidence that the relationship between T and sexual behavior is bi-directional (Escasa et al., 2011). We also have to recognize the limitations of a peripheral measure of T in assessing T status. In men and women, it is thought that a large proportion of androgens (and estrogens) are produced within cells where they exert their action and circulating androgens do not reflect this ‘intracrine’ androgen synthesis (Labrie, 1991). Relatedly, different forms of the androgen receptor are thought to vary in their sensitivity to T (Wåhlin-Jacobsen et al., 2018). Hence, circulating T is only part of a complex picture.

Our study contributes toward addressing the deficit in terms of attention paid to the role of T in women’s sexuality (Bancroft & Graham, 2011) and the sparsity of data on the differences between men and women in the relationship between T and sexual function and behavior. Our data tend to confirm that differences between men and women need to be understood by examining them in the context of both social and hormonal influences on sexual function and behavior.